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1.
Int J Mol Sci ; 22(21)2021 Nov 08.
Artigo em Inglês | MEDLINE | ID: mdl-34769511

RESUMO

The hippocampus has long been considered as a key structure for memory processes. Multilevel alterations of hippocampal function have been identified as a common denominator of memory impairments in a number of psychiatric and neurodegenerative diseases. For many years, the glutamatergic and cholinergic systems have been the main targets of therapeutic treatments against these symptoms. However, the high rate of drug development failures has left memory impairments on the sideline of current therapeutic strategies. This underscores the urgent need to focus on new therapeutic targets for memory disorders, such as type 4 serotonin receptors (5-HT4Rs). Ever since the discovery of their expression in the hippocampus, 5-HT4Rs have gained growing interest for potential use in the treatment of learning and memory impairments. To date, much of the researched information gathered by scientists from both animal models and humans converge on pro-mnesic and anti-amnesic properties of 5-HT4Rs activation, although the mechanisms at work require more work to be fully understood. This review addresses a fundamental, yet poorly understood set of evidence of the potential of 5-HT4Rs to re-establish or limit hippocampal alterations related to neurological diseases. Most importantly, the potential of 5-HT4Rs is translated by refining hypotheses regarding the benefits of their activation in memory disorders at the hippocampal level.


Assuntos
Hipocampo/efeitos dos fármacos , Aprendizagem/fisiologia , Transtornos da Memória/tratamento farmacológico , Memória/fisiologia , Plasticidade Neuronal/fisiologia , Receptores 5-HT4 de Serotonina/química , Antagonistas da Serotonina/farmacologia , Animais , Hipocampo/metabolismo , Humanos , Transtornos da Memória/metabolismo , Transtornos da Memória/patologia , Receptores 5-HT4 de Serotonina/metabolismo
2.
Psychopharmacology (Berl) ; 238(10): 2883-2893, 2021 Oct.
Artigo em Inglês | MEDLINE | ID: mdl-34173033

RESUMO

RATIONALE: Tramadol is widely used for pain relief especially in seniors. However, long-term use of tramadol has serious adverse effects, including cognitive impairment. Besides its memory effects, already demonstrated in animals, a recent clinical report suggests that tramadol could also affect executive function in seniors. Several studies have hypothesized that the anti-muscarinic properties of tramadol could be responsible for the deleterious effects of tramadol on cognition. OBJECTIVES: We aimed at investigating the effects of chronic administration of tramadol on cognitive flexibility in adult male mice, as assessed by a visual discrimination reversal task using a touchscreen device. The effects of tramadol were further compared to those of scopolamine, a reference muscarinic antagonist. RESULTS: We found that, during the early phase of the reversal task, when cognitive flexibility is most in demand, both tramadol-treated mice (20 mg/kg, s.c., twice a day) and scopolamine-treated mice (0.5 mg/kg, s.c., twice a day) needed more correction trials and showed a higher perseveration index than saline-treated mice. Therefore, tramadol affects cognitive flexibility, and its anticholinergic properties could be at least partly involved in these deficits. CONCLUSIONS: In view of these deleterious cognitive effects of tramadol, physicians should be cautious when prescribing this analgesic, especially in seniors who are more vulnerable to adverse drug events and in which alternative prescription should be preferred whenever possible.


Assuntos
Tramadol , Animais , Cognição , Discriminação Psicológica , Masculino , Camundongos , Escopolamina/farmacologia , Tramadol/farmacologia , Percepção Visual
3.
Cereb Cortex ; 31(1): 694-701, 2021 01 01.
Artigo em Inglês | MEDLINE | ID: mdl-32935845

RESUMO

The type 4 serotonin receptor (5-HT4R) is highly involved in cognitive processes such as learning and memory. Behavioral studies have shown a beneficial effect of its activation and conversely reported memory impairments by its blockade. However, how modulation of 5HT4R enables modifications of hippocampal synaptic plasticity remains elusive. To shed light on the mechanisms at work, we investigated the effects of the 5-HT4R agonist RS67333 on long-term potentiation (LTP) within the hippocampal CA1 area. Although high-frequency stimulation-induced LTP remained unaffected by RS67333, the magnitude of LTP induced by theta-burst stimulation was significantly decreased. This effect was blocked by the selective 5-HT4R antagonist RS39604. Further, 5-HT4R-induced decrease in LTP magnitude was fully abolished in the presence of bicuculline, a GABAAR antagonist; hence, demonstrating involvement of GABA neurotransmission. In addition, we showed that the application of a GABABR antagonist, CGP55845, mimicked the effect of 5-HT4R activation, whereas concurrent application of CGP55845 and RS67333 did not elicit an additive inhibition effect on LTP. To conclude, through investigation of theta burst induced functional plasticity, we demonstrated an interplay between 5-HT4R activation and GABAergic neurotransmission within the hippocampal CA1 area.


Assuntos
Região CA1 Hipocampal/fisiologia , Potenciação de Longa Duração/fisiologia , Plasticidade Neuronal/fisiologia , Receptores 5-HT4 de Serotonina/metabolismo , Animais , Estimulação Elétrica/métodos , Potenciais Pós-Sinápticos Excitadores/fisiologia , Hipocampo/fisiologia , Masculino , Camundongos
4.
Cereb Cortex ; 31(1): 620-634, 2021 01 01.
Artigo em Inglês | MEDLINE | ID: mdl-32959057

RESUMO

Cognitive decline appears across aging. While some studies report beneficial effects of musical listening and practice on cognitive aging, the underlying neurobiological mechanisms remain unknown. This study aims to determine whether chronic (6 h/day, 3 times/week) and long-lasting (4-8 months) music exposure, initiated at middle age in rats (15 months old), can influence behavioral parameters sensitive to age effects and reduce age-related spatial memory decline in rats. Spontaneous locomotor, circadian rhythmic activity, and anxiety-like behavior as well as spatial working and reference memory were assessed in 14-month-old rats and then after 4 and 8 months of music exposure (19 and 23 months old, respectively). Spatial learning and reference memory data were followed up by considering cognitive status of animals prior to music exposure (14 months old) given by K-means clustering of individual Z-score. Hippocampal cell proliferation and brain-derived neurotrophic factor (BDNF) level in the hippocampus and frontal cortex were measured. Results show that music exposure differentially rescues age-related deficits in spatial navigation tasks according to its duration without affecting spontaneous locomotor, circadian rhythmic activity, and anxiety-like behavior. Hippocampal cell proliferation as well as hippocampal and frontal cortex BDNF levels was not affected by music across aging. Cognitive improvement by music in aging rats may require distinct neurobiological mechanisms than hippocampal cell proliferation and BDNF.


Assuntos
Envelhecimento/fisiologia , Transtornos Cognitivos/prevenção & controle , Disfunção Cognitiva/prevenção & controle , Música , Tempo , Animais , Ansiedade/psicologia , Cognição/fisiologia , Transtornos Cognitivos/fisiopatologia , Hipocampo/fisiologia , Hipocampo/fisiopatologia , Masculino , Neurogênese/fisiologia , Ratos Wistar , Aprendizagem Espacial/fisiologia
5.
Schizophr Res ; 228: 519-528, 2021 02.
Artigo em Inglês | MEDLINE | ID: mdl-33298334

RESUMO

Whether the etiology of schizophrenia remains unknown, its multifactorial aspect is conversely now well admitted. However, most preclinical models of the disease still rely on a mono-factorial construction and do not allow discover unequivocal treatments, particularly for negative and cognitive symptoms. The main interaction factors that have been implicated in schizophrenia are a genetic predisposition and unfavorable environmental factors. Here we propose a new animal model combining a genetic predisposition (1st hit: partial deletion of MAP-6 (microtubule-associated protein)) with an early postnatal stress (2nd hit: 24 h maternal separation at post-natal day 9), and a late cannabinoid exposure during adolescence (3rd hit: tetrahydrocannabinol THC from post-natal day 32 to 52; 8 mg/kg/day). The 2-hit mice displayed spatial memory deficits, decreased cortical thickness and fractional anisotropy of callosal fibers. The 3-hit mice were more severely affected as attested by supplementary deficits such a decrease in spontaneous activity, sociability-related behavior, working memory performances, an increase in anxiety-like behavior, a decrease in hippocampus volume together with impaired integrity of corpus callosum fibers (less axons, less myelin). Taken together, these results show that the new 3-hit model displays several landmarks mimicking negative and cognitive symptoms of schizophrenia, conferring a high relevance for research of new treatments. Moreover, this 3-hit model possesses a strong construct validity, which fits with gene x environment interactions hypothesis of schizophrenia. The 2-hit model, which associates maternal separation with THC exposure in wild-type mice gives a less severe phenotype, and could be useful for research on other forms of psychiatric diseases.


Assuntos
Esquizofrenia , Animais , Modelos Animais de Doenças , Interação Gene-Ambiente , Hipocampo , Privação Materna , Camundongos , Esquizofrenia/genética
6.
Exp Gerontol ; 106: 222-231, 2018 06.
Artigo em Inglês | MEDLINE | ID: mdl-29524468

RESUMO

Episodic memory decline is one of the earlier deficits occurring during normal aging in humans. The question of spatial versus non-spatial sensitivity to age-related memory decline is of importance for a full understanding of these changes. Here, we characterized the effect of normal aging on both non-spatial (object) and spatial (object location) memory performances as well as on associated neuronal activation in mice. Novel-object (NOR) and object-location (OLR) recognition tests, respectively assessing the identity and spatial features of object memory, were examined at different ages. We show that memory performances in both tests were altered by aging as early as 15 months of age: NOR memory was partially impaired whereas OLR memory was found to be fully disrupted at 15 months of age. Brain activation profiles were assessed for both tests using immunohistochemical detection of c-Fos (neuronal activation marker) in 3and 15 month-old mice. Normal performances in NOR task by 3 month-old mice were associated to an activation of the hippocampus and a trend towards an activation in the perirhinal cortex, in a way that did significantly differ with 15 month-old mice. During OLR task, brain activation took place in the hippocampus in 3 month-old but not significantly in 15 month-old mice, which were fully impaired at this task. These differential alterations of the object- and object-location recognition memory may be linked to differential alteration of the neuronal networks supporting these tasks.


Assuntos
Envelhecimento/fisiologia , Hipocampo/fisiopatologia , Aprendizagem em Labirinto , Reconhecimento Psicológico/fisiologia , Memória Espacial , Animais , Comportamento Exploratório , Feminino , Camundongos , Proteínas Proto-Oncogênicas c-fos/metabolismo
7.
Neurosci Biobehav Rev ; 68: 979-1000, 2016 Sep.
Artigo em Inglês | MEDLINE | ID: mdl-27344000

RESUMO

Sex is often overlooked in animal and human research. Cognitive impairment associated with schizophrenia (CIAS) remains an unmet clinical need, as current antipsychotic medication does not provide clinically meaningful improvements. One explanation could be lack of appreciation of gender differences in CIAS. Animal models play a critical role in drug development and improved translation to the clinic is an on-going process. Our systematic review aims to evaluate how well the animal studies translate into clinical findings. Supporting clinical results, our review highlights a male working memory advantage and a female advantage for visual memory and social cognition in rodent models for schizophrenia. Not investigated in animals, a female advantage for attention and speed of processing has been found in schizophrenia patients. Sex differences in reasoning and problem solving are poorly investigated in both human and animal studies. Overall, our review provides evidence of good translation from the animal models into the clinic when sexual dimorphism is assessed. Enhanced understanding of these sex differences will improve the management of CIAS.


Assuntos
Cognição , Esquizofrenia , Animais , Transtornos Cognitivos , Feminino , Humanos , Masculino , Testes Neuropsicológicos , Psicologia do Esquizofrênico , Caracteres Sexuais
8.
Behav Brain Res ; 286: 80-4, 2015 Jun 01.
Artigo em Inglês | MEDLINE | ID: mdl-25732955

RESUMO

A common trait of numerous memory disorders is the impairment of episodic memory. Episodic memory is a delay-dependant memory, especially associating three components, the "what", "where" and "when" of a unique event. To investigate underlying mechanisms of such memory, several tests, mainly based on object exploration behaviour, have been set up in rodents. Recently, a three-trial object recognition task has been proposed to evaluate simultaneously the different components of episodic-like memory in rodents. However, to date, the time course of each memory component in this paradigm is not known. We characterised here the time course of memory decay in adult mice during the three-trial object recognition task, with inter-trial interval (ITI) ranging from 1h to 4h. We found that, with 1h and 2h, but not 4h ITI, mice spent more time to explore the displaced "old object" relative to the displaced "recent object", reflecting memory for "what and when". Concomitantly, animals exhibited more exploration time for the displaced "old object" relative to the stationary "old object", reflecting memory for "what and where". These results provide strong evidence that mice establish an integrated memory for unique experience consisting of the "what", "where" and "when" that can persist until 2h ITI.


Assuntos
Memória Episódica , Camundongos/psicologia , Reconhecimento Psicológico , Memória Espacial , Percepção do Tempo , Análise de Variância , Animais , Comportamento Exploratório , Masculino , Testes Neuropsicológicos , Testes Psicológicos , Fatores de Tempo
9.
Cereb Cortex ; 25(11): 4048-61, 2015 Nov.
Artigo em Inglês | MEDLINE | ID: mdl-24904072

RESUMO

Environmental enrichment is a powerful way to stimulate brain and behavioral plasticity. However the required exposure duration to reach such changes has not been substantially analyzed. We aimed to assess the time-course of appearance of the beneficial effects of enriched environment. Thus, different behavioral tests and neurobiological parameters (such as neurogenesis, brain monoamines levels, and stress-related hormones) were concomitantly realized after different durations of enriched environment (24 h, 1, 3, or 5 weeks). While short enrichment exposure (24 h) was sufficient to improve object recognition memory performances, a 3-week exposure was required to improve aversive stimulus-based memory performances and to reduce anxiety-like behavior; effects that were not observed with longer duration. The onset of behavioral changes after a 3-week exposure might be supported by higher serotonin levels in the frontal cortex, but seems independent of neurogenesis phenomenon. Additionally, the benefit of 3-week exposure on memory was not observed 3 weeks after cessation of enrichment. Thus, the 3-week exposure appears as an optimal duration in order to induce the most significant behavioral effects and to assess the underlying mechanisms. Altogether, these results suggest that the duration of exposure is a keystone of the beneficial behavioral and neurobiological effects of environmental enrichment.


Assuntos
Encéfalo/fisiologia , Meio Ambiente , Neurogênese/fisiologia , Plasticidade Neuronal/fisiologia , Reconhecimento Fisiológico de Modelo/fisiologia , Animais , Aprendizagem da Esquiva/fisiologia , Monoaminas Biogênicas/metabolismo , Encéfalo/citologia , Bromodesoxiuridina , Proliferação de Células/fisiologia , Corticosterona/sangue , Comportamento Exploratório/fisiologia , Elevação dos Membros Posteriores , Masculino , Aprendizagem em Labirinto/fisiologia , Camundongos , Transtornos do Humor/fisiopatologia , Natação , Fatores de Tempo
10.
Behav Brain Res ; 285: 176-93, 2015 May 15.
Artigo em Inglês | MEDLINE | ID: mdl-25447293

RESUMO

The novel object recognition test (NOR) test is a two trial cognitive paradigm that assesses recognition memory. Recognition memory is disturbed in a range of human disorders and NOR is widely used in rodents for investigating deficits in a variety of animal models of human conditions where cognition is impaired. It possesses several advantages over more complex tasks that involve lengthy training procedures and/or food or water deprivation. It is quick to administer, non-rewarded, provides data quickly, cost effective and most importantly, ethologically relevant as it relies on the animal's natural preference for novelty. A PubMed search revealed over 900 publications in rats and mice using this task over the past 3 years with 34 reviews in the past 10 years, demonstrating its increasing popularity with neuroscientists. Although it is widely used in many disparate areas of research, no articles have systematically examined this to date, which is the subject of our review. We reveal that NOR may be used to study recognition memory deficits that occur in Alzheimer's disease and schizophrenia, where research is extensive, in Parkinson's disease and Autism Spectrum Disorders (ASD) where we observed markedly reduced numbers of publications. In addition, we review the use of NOR to study cognitive deficits induced by traumatic brain injury and cancer chemotherapy, not disorders per se, but situations in which cognitive deficits dramatically reduce the quality of life for those affected, see Fig. 1 for a summary. Our review reveals that, in all these animal models, the NOR test is extremely useful for identification of the cognitive deficits observed, their neural basis, and for testing the efficacy of novel therapeutic agents. Our conclusion is that NOR is of considerable value for cognitive researchers of all disciplines and we anticipate that its use will continue to increase due to its versatility and several other advantages, as detailed in this review.


Assuntos
Transtornos Cognitivos/diagnóstico , Testes Psicológicos , Reconhecimento Psicológico , Animais , Modelos Animais de Doenças , Camundongos , Ratos
11.
Behav Brain Res ; 266: 188-92, 2014 Jun 01.
Artigo em Inglês | MEDLINE | ID: mdl-24632009

RESUMO

Recognition memory, impaired in neuropsychiatric conditions and currently untreated, may be assessed by the novel object recognition (NOR) task with robust impairments induced by sub-chronic treatment with the N-methyl-d-aspartate receptor antagonist phencyclidine (PCP). The aim of the present study was to investigate how sub-chronic PCP produces its effects in this task. Forty adult female rats received vehicle or PCP (2mg/kg i.p. twice daily for 7 days followed by 7 days washout). Rats completed a 3-min acquisition trial followed by differential inter-trial-interval (ITI) conditions (1 min in the home cage, 10s in the home cage, 1 min in the NOR test box in the presence of an unfamiliar object or 1 min in the NOR test box completely undisturbed) followed by a 3-min retention trial. Control rats spent significantly more time exploring the novel compared with the familiar object in retention. This effect was abolished in the sub-chronic PCP treated animals following all ITI conditions except in rats left completely undisturbed in the NOR test box for a 1 min ITI. The combined influence of sub-chronic PCP treatment and the effect of distraction provides further support for the validity of the NOR test in mimicking cognitive deficits of relevance to schizophrenia.


Assuntos
Antagonistas de Aminoácidos Excitatórios/toxicidade , Transtornos da Memória/induzido quimicamente , Fenciclidina/toxicidade , Reconhecimento Psicológico/efeitos dos fármacos , Análise de Variância , Animais , Modelos Animais de Doenças , Comportamento Exploratório/efeitos dos fármacos , Feminino , Atividade Motora/efeitos dos fármacos , Ratos , Fatores de Tempo
12.
Nat Protoc ; 8(12): 2531-7, 2013 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-24263092

RESUMO

The object recognition test is now among the most commonly used behavioral tests for mice. A mouse is presented with two similar objects during the first session, and then one of the two objects is replaced by a new object during a second session. The amount of time taken to explore the new object provides an index of recognition memory. As more groups have used the protocol, the variability of the procedures used in the object recognition test has increased steadily. This protocol provides a necessary standardization of the procedure. This protocol reduces inter-individual variability with the use of a selection criterion based on a minimal time of exploration for both objects during each session. In this protocol, we describe the three most commonly used variants, containing long (3 d), short (1 d) or no habituation phases. Thus, with a short intersession interval (e.g., 6 h), this procedure can be performed in 4, 2 or 1 d, respectively, according to the duration of the habituation phase. This protocol should allow for the comparison of results from different studies, while permitting adaption of the protocol to the constraints of the experimenter.


Assuntos
Camundongos/psicologia , Reconhecimento Psicológico , Animais , Habituação Psicofisiológica , Manobra Psicológica , Memória , Fatores de Tempo
13.
PLoS One ; 7(10): e48043, 2012.
Artigo em Inglês | MEDLINE | ID: mdl-23110171

RESUMO

Although environmental enrichment is well known to improve learning and memory in rodents, the underlying neuronal networks' plasticity remains poorly described. Modifications of the brain activation pattern by enriched condition (EC), especially in the frontal cortex and the baso-lateral amygdala, have been reported during an aversive memory task in rodents. The aims of our study were to examine 1) whether EC modulates episodic-like memory in an object recognition task and 2) whether EC modulates the task-induced neuronal networks. To this end, adult male mice were housed either in standard condition (SC) or in EC for three weeks before behavioral experiments (n = 12/group). Memory performances were examined in an object recognition task performed in a Y-maze with a 2-hour or 24-hour delay between presentation and test (inter-session intervals, ISI). To characterize the mechanisms underlying the promnesiant effect of EC, the brain activation profile was assessed after either the presentation or the test sessions using immunohistochemical techniques with c-Fos as a neuronal activation marker. EC did not modulate memory performances after a 2 h-ISI, but extended object recognition memory to a 24 h-ISI. In contrast, SC mice did not discriminate the novel object at this ISI. Compared to SC mice, no activation related to the presentation session was found in selected brain regions of EC mice (in particular, no effect was found in the hippocampus and the perirhinal cortex and a reduced activation was found in the baso-lateral amygdala). On the other hand, an activation of the hippocampus and the infralimbic cortex was observed after the test session for EC, but not SC mice. These results suggest that the persistence of object recognition memory in EC could be related to a reorganization of neuronal networks occurring as early as the memory encoding.


Assuntos
Meio Ambiente , Aprendizagem em Labirinto/fisiologia , Memória/fisiologia , Neurônios/fisiologia , Animais , Comportamento Exploratório/fisiologia , Hipocampo/citologia , Hipocampo/metabolismo , Hipocampo/fisiologia , Abrigo para Animais , Imuno-Histoquímica , Masculino , Camundongos , Camundongos Endogâmicos , Plasticidade Neuronal , Neurônios/metabolismo , Proteínas Proto-Oncogênicas c-fos/metabolismo , Reconhecimento Psicológico/fisiologia , Fatores de Tempo
14.
Behav Brain Res ; 230(1): 78-84, 2012 Apr 21.
Artigo em Inglês | MEDLINE | ID: mdl-22326698

RESUMO

Whereas severe hypoxia is known to contribute to neuronal death and to lead to neurological disturbances, mild hypoxia can also induce beneficial effects through endogenous adaptive responses. The aim of this study was to investigate the effects of mild hypoxia (8% O(2)) on cognitive and emotional behavior in the adult mouse. To this end, mice were submitted to repeated mild hypoxia exposure or normoxia during 6 weeks and underwent behavioral testing during the last 3 weeks. Hypoxia decreased anxiety-like behavior in the light/dark transition test, enhanced, albeit modestly, non-spatial recognition memory, but did not alter spontaneous locomotor activity, nor spatial learning. On additional mice, whole brain adrenomedullin mRNA expression was found to be increased at D1, D25 and D41 after hypoxia initiation and vascular endothelial growth factor (VEGF) mRNA expression was increased at only on D41. This work shows that repeated mild hypoxic exposure decreases anxiety-related behavior and points out hypoxia inducible factor-1 (HIF-1) target genes, particularly adrenomedullin, as potential mediator candidate.


Assuntos
Adrenomedulina/metabolismo , Transtornos de Ansiedade/fisiopatologia , Encéfalo/metabolismo , Regulação da Expressão Gênica/fisiologia , Hipóxia/patologia , Hipóxia/fisiopatologia , Adrenomedulina/genética , Análise de Variância , Animais , Fator 1 Induzível por Hipóxia/genética , Fator 1 Induzível por Hipóxia/metabolismo , Locomoção/fisiologia , Masculino , Aprendizagem em Labirinto/fisiologia , Camundongos , RNA Mensageiro/metabolismo , Reconhecimento Psicológico/fisiologia , Fatores de Tempo , Fator A de Crescimento do Endotélio Vascular/genética , Fator A de Crescimento do Endotélio Vascular/metabolismo
15.
Behav Brain Res ; 228(1): 22-9, 2012 Mar 01.
Artigo em Inglês | MEDLINE | ID: mdl-22138509

RESUMO

Environmental enrichment is known to improve learning and memory in adult rodents. Whereas the morphological changes underlying these beneficial effects are well documented, few studies have addressed the influence of this housing condition on the neuronal networks underlying memory processes. We assessed the effects of environmental enrichment on behavioural performances and brain metabolic activation during a memory task in mice. Adult mice were housed in standard (SC) or enriched (EC) conditions for 3 weeks. Then, recent and remote memory performances were measured in the passive avoidance test. After testing, brain metabolic activation was assessed through cytochrome oxidase (CO) activity. EC improved recent memory, in association with an increased metabolic activation in the frontal and prefrontal cortices and a decreased activation in the baso-lateral amygdala and the hippocampus. EC did not improve remote memory, and globally decreased CO activity. Our findings suggest the involvement of regions of pivotal importance during recent memory, such as the frontal cortex, in the beneficial effects of EC.


Assuntos
Encéfalo/metabolismo , Complexo IV da Cadeia de Transporte de Elétrons/metabolismo , Meio Ambiente , Memória de Longo Prazo/fisiologia , Memória de Curto Prazo/fisiologia , Animais , Animais não Endogâmicos , Aprendizagem da Esquiva/fisiologia , Abrigo para Animais , Masculino , Camundongos
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